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Legume-supported cropping systems for Europe (Legume Futures) is a collaborative research project funded from the European Union’s Seventh Programme for research, technological development and demonstration under grant number 245216

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Legume Futures Report 1.5

Biological nitrogen fixation (BNF) by legume crops in Europe

Compiled by:

J.A. Baddeley, S. Jones, C.F.E. Topp and C.A. Watson

Scotland’s Rural College

J. Helming

Wageningen University and Research Centre; and

F.L. Stoddard

University of Helsinki

February 2014

Legume-supported cropping systems for Europe

Legume Futures Report 1.5:

Biological nitrogen fixation (BNF) in Europe

2

Legume Futures

Legume-supported cropping systems for Europe (Legume Futures) is an international

research project funded from the European Union’s Seventh Programme for research,

technological development and demonstration under grant agreement number

245216. The Legume Futures research consortium comprises 20 partners in 13 countries.

Disclaimer

The information presented here has been thoroughly researched and is believed to be

accurate and correct. However, the authors cannot be held legally responsible for any

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Citation

Please cite this report as follows:

Baddeley, J.A., Jones, S., Topp, C.F.E., Watson, C.A., Helming, J. & Stoddard, F.L. 2013.

Biological nitrogen fixation (BNF) by legume crops in Europe. Legume Futures Report 1.5.

Available from www.legumefutures.de




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CONTENTS

ABBREVIATIONS ...................................................................................................................................................... 4

INTRODUCTION ....................................................................................................................................................... 5

METHODS ................................................................................................................................................................ 7

FORAGE LEGUMES ............................................................................................................................................................... 7

GRAIN LEGUMES ................................................................................................................................................................. 7

RESULTS .................................................................................................................................................................. 9

DISCUSSION ........................................................................................................................................................... 14

APPROACH ...................................................................................................................................................................... 14

FORAGE LEGUMES ............................................................................................................................................................. 14

GRAIN LEGUMES ............................................................................................................................................................... 15

N BALANCE ...................................................................................................................................................................... 15

BNF IN EUROPE ............................................................................................................................................................... 16

PROBLEMS AND LIMITATIONS .............................................................................................................................................. 16

CONCLUSIONS ....................................................................................................................................................... 17

SUPPLEMENTARY TABLES ...................................................................................................................................... 21




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ABBREVIATIONS

BNF Biological nitrogen fixation

kfix country-specific biological fixation coefficient for forage legumes

Ndfa Proportion of nitrogen derived from the atmosphere




5

INTRODUCTION

Biological nitrogen fixation (BNF) is the distinguishing feature of a legume in a cropping

system. Most legume species are able to form a symbiosis with alpha- or beta-

proteobacteria, collectively called rhizobia, that use solar energy captured by the plant to

break the bond in inert atmospheric dinitrogen and form reactive N species, initially

ammonium (NH4+). As a result of this symbiosis, the legume crop requires little or no input

of N fertilizer and makes little demand on soil N reserves. Since the manufacture of

synthetic fertilizer consumes fossil fuel, thereby releasing CO2, and the transport and

spreading of organic and synthetic N fertilizers consumes further fuel, the use of legumes

in cropping systems has immediate environmental benefits arising from reduced fossil fuel

use. Nitrates from fertilizers and soil N reserves may also leach through the soil column

into groundwater, and the denitrification of nitrates from synthetic or organic sources is the

primary source of nitrous oxide (N2O), a powerful greenhouse gas, from agricultural soils

(Philippot and Hallin 2011). Hence maintaining the reactive N within the plant, as happens

in a symbiotic legume in the growing season, avoids some potential for environmental

damage.

Crop residues of legumes contain some of the N that they have fixed, and this becomes

available to subsequent crops. These residues are considered just as likely to contribute

to leaching or N2O release as any other crop residue (see the Legume Futures report on

N2O), but a portion of the fixed N remains in the soil/plant system reducing N fertilizer

needs in subsequent crops.

Depending on the genetic constitution of the rhizobium, hydrogen may be released during

N fixation (Golding & Dong 2010). This gas stimulates the growth of hydrogen-fixing

bacteria in the rhizosphere, and these compete successfully for living space with other

rhizosphere organisms, including many pathogens. Some of the hydrogen bacteria have

plant growth-promoting properties (Maimaiti et al. 2007). Thus the use of BNF leads to

positive changes in the structure of the soil microbiological community.

Large, continental- or global-scale estimates of BNF have been attempted. Yang et al.

(2010) used a range of national databases to compile an estimate of BNF in Canada. An

Australian estimate also used national databases, and noted that below-ground residues

were not included (Unkovich et al. 2010). A global estimate factored in below-ground

residues and highlighted some of the other uncertainties in the process (Herridge et al.

2008). Chief amongst these uncertainties is the amount of N fixed by crops. A recent

attempt to produce a high-resolution assessment of global N flows in cropland cited one of

the main limitations of their method as the lack of crop-specific N fixation data (Liu et al.,

2010a). This was highlighted by their use of N fixation figures from Smil (1999), who had

commented on their own use of unreliable data on average annual BNF rates of important

species and cultivars.




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For these reasons, we set out to develop an improved estimate for BNF across Europe.

BNF is usually quoted on a kg ha-1 basis from experiments conducted in a limited area and

time, and datasets from a wide range of crops and growing conditions show a wide range

in amounts fixed, depending especially on biomass and available soil N. Previous

attempts to estimate N fixation have tended to follow a common approach in that they

calculate the amount of N fixed as the as the product of the land area cultivated and

fixation per area. The figures for the former are obtained from published databases such

as FAOstat and, subject to the level of detail made available about data collection

methods, are taken at face value. In contrast, data on N fixation range hugely for each

legume species depending on growing conditions, in particular biomass production and

available soil nitrogen. Yields range more than 10-fold across species, countries and

years. Thus we took the approach that it is not desirable simply to use legume areas for

each country and convert these to overall fixed N using an average figure for BNF. Hence

we attempted to take a stepwise approach using the most detailed available data and

robust scientific logic.

Most legume crops maintain their N concentration within a relatively narrow physiological

range. This is true across a 10-fold range of overall biomass yields, for annual grain

legumes (Evans et al., 1989; Pilbeam et al., 1997; Unkovich et al., 2010) and for perennial

forage legumes (Carlsson and Huss-Danell 2003). In most circumstances, a legume with

its rhizobia can fix its own N, so growth of the crop is unlikely to be limited by N supply.

Rather, crop N yield is likely to reflect overall crop yield as limited by other factors,

including rainfall and temperature.

Grain yields of the grain legumes can be used to estimate biomass by using data on

harvest index and root:shoot ratio, and sufficient data are available on N concentrations in

seeds, straw and roots of the main species to allow N yields to be calculated. Further

factors to be considered are rhizodeposition, the deposition of N in the root zone from

dead cells, root exudates, and shed fragments of roots (Fustec et al. 2010) and the

amount of N derived from fixation.

In contrast, data on yields of fodder/forage legumes and legume-grass systems (hereafter

“forage legumes”), and their legume content, are not available in any systematic way.

Furthermore, the moisture content of the yields that are published on FAOstat is not clear,

while that in Eurostat is stated as 65%. The CAPRI model allows some estimation of

biological N fixation based on Eurostat data on the areas of forages per country (Britz and

Witzke, 2012). Yields of grazed pastures are not estimated in any database.

Thus we have adopted different methodologies for estimating BNF by grain and forage

legumes.




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METHODS

Forage legumes

BNF of forage legumes was estimated for each country in the EU27 as the product of crop

area, N retention, and biological fixation coefficient. Crop areas were obtained from

Eurostat. N retention (N in plant biomass) was obtained from the Common Agricultural

Policy Regionalised Impact (CAPRI) model, an economic model for agriculture focussed

on Europe, which uses input data mainly compiled from official Eurostat data (Britz and

Witzke, 2008). The latest complete dataset within CAPRI is from 2009, so datasets from

that year were used. The biological fixation coefficients (kfix) are determined by the N fixed

per hectare and the proportion of the grassland that is assumed to include a legume

component.

The current version of CAPRI accounts for the share of forage legumes in all grasslands,

but after an initial round of calculations, the predicted N fixation values were considered to

be too high. Consequently, the proportions of forage legumes in these systems were re-

estimated in collaboration with colleagues in the Legume Futures network and checked, as

far as possible, with Eurostat data. This process, which follows the approach

recommended by Eurostat to improve estimates of BNF in grasslands (Eurostat, 2013) led

to the derivation of revised figures for kfix that are used in this study.

Grain legumes

Data on areas and yields of grain legumes were taken from FAOstat (FAOstat 2014), as

this differentiates more individual crops than Eurostat. Only classes that represent

agricultural production of grain legumes harvested for dry grains were included (defined in

Table 1), because production of horticultural legumes such as vining pea is generally high-

input and seldom relies on BNF. Cowpea was excluded as annual production in EU27 is

less than 200 t and there is very little available data on N partitioning. There are some

inconsistencies between FAOstat and Eurostat in the major grain legume crops, especially

a misallocation of UK faba bean to "pulses" instead of "broad beans, dry", so the areas of

pea, faba bean, lupins and soya were taken from Eurostat, while those of lentil, chickpea,

common bean and vetches were taken from FAOstat.

The production data generally represent mass at commercial moisture content, which we

taken as 14%. To convert these production figures to above-ground biomass production,

the harvest index of each crop was used. This value is fairly consistent within each

species, although extreme values can be found in exceptional growing conditions. Above-

ground biomass was then converted into above-ground N yield by first converting the

widely available data on average grain protein concentration to grain N concentration




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using the standard conversion factor of 5.60 (Sosulski and Holt, 1980; Mariotti et al., 2008).

This, divided by the N harvest index, gives the above-ground N yield.

Accurate determination of root biomass production is notoriously difficult as it is hard to

quantitatively separate roots from field soils, and root tissues tend to die as an annual crop

reaches harvest maturity. Although some previous studies have assumed root biomass to

be a constant proportion of above-ground biomass, here we adopted a species-specific

approach using root:shoot ratios that are obtainable for many species based on mid-

season growth when living root mass is at its maximum. From above-ground biomass and

root:shoot ratio, root biomass was calculated. Root N yield was then calculated using root

biomass and values of root N concentration from the literature, where available. While

root N yield is lower than above-ground N yield, our calculations show that it is important.

Table 1. Definitions of grain legume categories used by FAO and included in this study.

Cowpea and horticulturally produced vegetable legumes were excluded from the analysis.

Name FAO Category Genus and species covered

Beans Beans, dry Phaseolus spp. and most Vigna spp.

Faba bean Broad beans,

horse beans, dry

Vicia faba

Chickpea Chick pea Cicer arietinum

Lentil Lentil Lens culinaris

Lupins Lupins Lupinus spp. (L. albus, L. angustifolius, L. luteus)

Pea Peas, dry Pisum sativum

Soya bean Soybeans Glycine max

Vetches Vetches Vicia species other than V. faba (mostly V. sativa)

Rhizodeposition is a relatively recent addition to the legume N budget, and covers

biomass left in the soil from root exudates, leachates, root-cap cells, and detached or dead

root fragments. Although it is hard to determine experimentally there are a few estimates

in the literature, usually given as proportional rhizodeposition, the proportion of plant N in

rhizodeposits relative to total or above-ground N. Here we use species-specific values

where available, otherwise the default of 0.15 (Mahieu et al., 2007; Wichern et al., 2008).

From this sequence of calculations, the total N production of a grain legume crop was

calculated, relative to its grain production. Converting this to an estimate of N fixation

required one more factor, namely the proportion of N derived from the atmosphere (Ndfa).

This figure may be as low as zero, when there is plentiful mineral N in the soil, the

appropriate symbiont is not available, or the legume-rhizobium symbiosis is ineffective. It

may also exceed 90% in the opposite circumstances. Thus Ndfa is the most sensitive




9

factor in estimating overall European BNF. Here we used values extracted from the

literature for the most typical agronomic conditions available, i.e., no or low levels of N

fertilizer addition. This gave a mean value of 63%, which is comparable with than that

used in other studies on this scale (e.g. 57%, Herridge et al., 2008) and is much lower

than the 75% used in CAPRI.

These figures, on a per-tonne-harvested basis, were then converted to totals for the EU27

countries, based on the grain production statistics for 2009, to be comparable with the

forage legume data.

RESULTS

Grain legumes in Europe were calculated to fix about 13 and 20 times more N per hectare

than temporary or permanent pastures respectively (Table 2). Although permanent

pastures had the lowest fixation rate per hectare, they were responsible for nearly half of

the total 811 Gg of N fixed across Europe (Figure 1). Total N fixation by grain legumes

was comparable with that of the temporary grasslands, although the area of grain legumes

grown is very much smaller (78 and 1.6 M ha respectively).

Across countries, the yields of N fixed in both temporary and permanent grassland

systems were smallest in Cyprus and highest in Denmark (Figure 1, with supporting data

in Supplementary Table 1). However, the total amounts of N fixed tended, not surprisingly,

to be determined by cultivated land areas. In temporary systems, Malta had the least N

fixation (9 t) and Italy the greatest (27.8 Gg). In permanent systems, the least N fixation

was in Cyprus (20 t) and the greatest in France (62.3 Gg).

Total N yield of the different grain legume crops ranged from 63.6 kg t-1 for pea to 106.9 kg

t-1 for soya bean (Table 3; full calculations shown in Supplementary Table 2). The

amounts of N fixed by each crop ranged from 28.4 kg t-1 for beans to 68.9 kg t-1 for lupins.

Finally, the N balance for each crop ranged from -9.4 kg t-1 for beans to 23.9 kg t-1 for faba

bean.

Table 2. Area-weighted mean N fixation (with standard deviation) and total N fixed in

temporary and permanent pastures and by grain legumes in the EU27 in 2009.

Temporary grassland Permanent grassland Grain legumes Total

Mean N fixation (kg ha-1) 10.1 (0.5) 6.8 (0.3) 133 (10)

Total N fixed (Gg) 172 414 225 811




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Table 3. Calculated quantities of total N production and N fixed, and overall N balance (N

fixed – N offtake) by grain legume crops EU27 in 2009. All figures are kg of N per tonne of

grain production. Full calculations are shown in Supplementary Table 2.

Common

bean

Faba

bean

Chick-

pea

Lentil Lupins Pea Soya

bean

Vetches

Total N

production 58.7 81.1 83.2 82.5 76.1 57.5 96.5 87.7

N fixed 26.0 62.4 41.6 57.7 62.4 40.2 50.2 63.2

N balance -7.9 22.2 11.6 18.1 13.3 5.8 -4.6 23.2

The calculated total amounts of N fixed by each grain legume crop across EU27 in 2009

are presented in Figure 2. In common with the results for forage legumes (Table 2), the

figures are largely a reflection of the areas of each crop grown, with the most N fixed by

pea and the least by chickpea. The total fixation of 225 Gg was dominated by 3 crops,

pea, faba bean and soya bean, which between them were responsible for about three

quarters of all N fixation. A large proportion of the total N was fixed by a fourth category of

crop, “pulses”, but this is an amalgamation of many minor grain legume species together

with varied reporting of some of the more common species.

The potential extent by which the N in cropping systems is being replenished or depleted

after the growth of grain legume crops is shown by the N balance data (Figure 3).

Common bean and soya bean have negative N balances of -1.1 and -4.6 Gg respectively,

indicating a net loss of N from these systems. All other grain legumes have positive N

balances with the greatest being for 18.4 Gg for faba bean.

The total amounts of N fixed by grain and forage legume systems per country show a

range of three orders of magnitude from 120 t in Malta and Cyprus to 151 Gg in France

(Figure 4). Nearly half of all N fixed in the EU27 is in three countries, France, Italy and UK.

Figure 4 also shows the large variation in the relative amounts N fixed by forage and grain

legumes in each country. In Ireland and Lithuania almost all fixation is by forage legumes

whereas in Austria, France and Latvia about 40% of fixation is by grain legumes.




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Figure 1. Calculated quantities of N fixed by forage legumes in temporary and permanent

pastures in the EU27 countries in 2009. Details are given in Supplementary Table 1.




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Figure 2. Calculated quantities of total N fixed (Gg) by grain legume crops across the

EU27 countries in 2009. Details are given in Supplementary Table 4.

Chickpea Common bean

Faba bean

Lentil Lupin Pea Soya bean

Vetches-5

0

5

10

15

20

25

30

35

N b

ala

nce

(G

g)

Figure 3. Calculated N balance (N fixed – N grain offtake) for grain legume crops across

the EU27 countries in 2009. Overall N balance was 36.6 Gg




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UK

Sweden

Spain

Slovenia

Slovak Rep

Romania

Portugal

Poland

Netherlands

Malta

Lithuania

Latvia

Italy

Ireland

Hungary

Greece

Germany

France

Finland

Estonia

Denmark

Czech Rep

Cyprus

Bulgaria

Belgium & Lux

Austria

0 20 40 60 80 100 120 140 160

N fixed (Gg)

Forage

Grain

Figure 4. Calculated quantities of N fixation by forage and grain legumes in EU27

countries in 2009. Detailed figures are provided in Supplementary Table 3.




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DISCUSSION

Approach

Any study that attempts to present an integrated estimate of agricultural N fixation will be

faced by the substantial difficulty of how to deal with the contribution from legumes in the

various types of forage systems. We took the basis for this element of the analysis from

outputs by the CAPRI model as it is an integral part of agricultural planning in the EU.

Until now, it has been difficult to derive reliable N fixation estimates from CAPRI as it has

required the use of databases that are not publicly accessible. To overcome this issue

and to make our estimates more accurate we, in conjunction with partners in the Legume

Futures network, derived new, country-specific fixation coefficients for temporary and

permanent pastures. This is an important modification in that it includes permanent

pastures, hitherto not included in the CAPRI model. This decision was vindicated by the

finding that these systems made the greatest contribution to total agricultural N fixation

across the EU, even though the per-hectare fixation was low. The decision to use a

species-specific model for the grain legumes was supported by the wide range of Ndfa

values found, in contrast to the fixed value of 75% in the CAPRI model. We can therefore

recommend that species-specific values be used in further developments of the CAPRI

model, at least for the major grain legumes that are separately itemized in the Eurostat

database, namely pea, faba bean, lupins and soya bean.

Forage legumes

Our fixation coefficients give slightly higher results than the figure of 5 kg ha-1 used in three

models that deal with N budgets in European agriculture (MNP, 2006; MITERRA, Velthof

et al 2009; INTEGRATOR, De Vries et al, 2011a). The difference is likely to be because

the figures we used accounted for the areas devoted to the growth of near-monocultures

of clovers and lucerne, which can fix considerable amounts of N. There is no indication of

how these are accounted for in other models. An attempt to estimate N fixation in

Canadian agriculture assumed N fixation of 4 kg ha-1 in improved and unimproved

pastures, but dealt with lucerne and hay (a mixture of clovers, lucerne and grasses)

systems separately (Yang et al., 2010). This approach was not practicable in the present

study because of the different ways that data are gathered in Canada and the EU. Data

on yields and areas of alfalfa, clovers and "other forage legumes" are available, at a stated

moisture content of 65% in Eurostat and an unknown moisture content in FAOstat. Data

on yields and areas of mixed forages such as grass-clover pastures, and their legume

content, are not available in any systematic way. Thus significant improvements in the

ability to predict N fixation in the permanent and temporary pasture and fodder systems

that are responsible for the majority of N fixed by European agriculture will only be

possible if more detailed and reliable production statistics become available.




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Grain legumes

Grain legume crops are grown almost exclusively as monocultures, so the issue of

estimating proportions, as alluded to above for forage legumes, is not a consideration.

This allowed the construction of a simple model of N partitioning in the main agricultural

grain legume species grown in Europe. This refines the concept of Peoples et al. (2009)

in that it relates fixation to readily available data on grain production, and it incorporates

the most recently available data on below-ground N partitioning and rhizodeposition.

The figures for N fixation by this novel approach compare closely with those used in other

studies of similar scope. Four European N budget models use amounts of N fixed

between 0.75 to 2.0 times the amount of harvested N for all grain legumes (2.0 in IMAGE,

MNP, 2006; 0.75 in IDEAg, Leip et al., 2008; 1.0 in MITERRA, Velthof et al., 2009; 1.2-1.3

in INTEGRATOR, De Vries et al., 2011a). The values calculated in this study ranged from

0.75 for beans to 1.53 for vetches and faba bean. A wide-ranging review concluded that

globally crop legumes fix an average of 20 kg of N per tonne of shoot biomass (Peoples et

al., 2009), which is in line with our values of 15 – 39 kg t-1.

N balance

Detailed prediction of the N partitioning in each grain legume crop also allowed the

prediction of N balance, the difference between N fixed and N removed in grain. This is

not the same as the N remaining after cropping, as it does not take into account mineral N

in the soil before cropping (N not derived from the atmosphere), and the processing of

crop residues varies widely in different systems. Nevertheless, positive values give a

useful indication of the potential input of atmospheric N to a system, whereas negative

values indicate an overall mining of soil N. As with the other values from the N partitioning

model, those for N balance compare well with experimental studies. As examples: for faba

bean the N balance related to shoot biomass was reported as 19 kg t-1 (Peoples et al.,

2009) and 9 kg t-1 (Vinther and Dahlmann-Hansen, 2005), compared to our value of 14

kg t-1. For lentils the N balance related to grain production was 18 kg t-1 (Kurdali et al.,

1997) and 25 kg t-1 (Schmidtke et al., 2004), compared to our value of 19 kg t-1. A meta-

analysis of 637 soya bean datasets found a partial N balance (based on aboveground N

only) of -17 kg t-1 of grain, compared with our value of -18 kg t-1.

While the growth of the majority of grain legumes results in potential N gains, negative

values were calculated for beans and soya bean, driven by low N fixation in the former and

high grain N content in the latter. The extent to which a negative balance is a problem in

practice is, however, questionable. Many experimental studies have found that growth of

both beans and soya bean can be beneficial to a following crop (e.g. Hesterman et al.,

1987; Bergersen et al., 1992; Green and Blackmer, 1995). Given that the growth of beans

and soya bean does not result in a net N increase in the system, it is likely that these




16

reported benefits are a result of other processes. These include promotion of the

mineralisation of soil organic matter, the so-called priming effect (Jenkinson et al, 1985;

Kuzyakov et al, 2000), and nitrate sparing, where the legume takes up less of the soil

nitrate than would a non-legume crop (Herridge et al 1995), as well as other legume-

specific and non-specific break crop effects (Legume Futures report 1.6). Thus while in

well managed, diverse rotations, the calculated negative N balance is probably sustainable,

monoculture of beans or soya bean is likely to be as unsustainable as any other

monoculture.

BNF in Europe

Overall, the calculated figure of 0.81 Mt of N fixed in EU27 by agricultural legumes in 2009

is broadly comparable with the mean estimate of 1.12 Mt from four European N budget

models (De Vries et al., 2011b) and the value of 1.1 Mt submitted to the United Nations

Framework Convention on Climate Change (EEA, 2008). Most of the difference occurs

because the N budget models allow for ~5 kg ha-1 of N fixation by free-living microbes in

all non-legume arable land, in contrast to our focus on legumes.

Problems and limitations

The greatest challenge to this exercise was to estimate BNF in forage systems, where the

yield is uncertain (especially in grazed systems), the legume content is unknown and

management is variable. Hence, we refined the use of area-based figures for N fixation as

far as possible by the derivation of new, country-specific constants for N fixation based on

expert opinion. Significant improvements to this would need more detailed data on land

areas under cultivation, their management, the proportion of legumes present and their

temporal variation. The collection of such data would require wide-ranging changes to the

way current agricultural statistics are collected, and this need has been recognised on the

Eurostat website: “The comparability and transparency of the estimation of BNF in

forage/fodder legumes and legume-grass mixtures could be improved if a set of common

guidelines on the estimation method and update frequency were established” (Eurostat,

2013).

In terms of the calculations of N fixed by grain legumes, the most sensitive figure is Ndfa.

The approach adopted here was to select literature values from a wide range of sources

constrained, where possible, to agronomic conditions that were appropriate for Europe.

Nevertheless, published values of Ndfa vary widely and depend on a complex set of

interacting factors such as existing and applied mineral N, presence of suitable rhizobia,

and efficiency of the plant-rhizobium symbiosis (e.g., Hardarson and Atkins, 2003;

Herridge et al, 2008). A further refinement to the present method would be to include

variables that are known to modify N fixation, such as soil N status, soil moisture, soil pH




17

and temperature, that are available from national institutions in Europe, and to use

constants that relate them to N fixation as they become available (Liu et al., 2010b).

CONCLUSIONS

The amount of N fixed by forage legumes and legume-grass systems was predicted by a

combination of outputs from the CAPRI model and improved, country-specific N fixation

coefficients. For grain legumes, the higher quality of available data made it possible to

construct a detailed model based on N partitioning. Both approaches predicted quantities

of N fixed that were broadly comparable with previously published estimates. Combining

these figures with published crop production statistics allowed the production of detailed

crop- and country-specific figures for N fixation by grain legumes that, for the first time,

took into account the large differences in yields across Europe. The results also showed

that while the amount of atmospheric N fixed into farming systems is likely to increase with

increasing cultivation of many species of grain legumes, this is unlikely for beans and soya

bean which apparently mine soil N reserves. Only minor adjustment to the Ndfa of soya

bean, through management or breeding, is required to make it a net contributor to the N

balance.

The results confirm that reliable estimates of agricultural N fixation in Europe require

accurate crop production and yield statistics. Estimating N fixation would be greatly

facilitated by changes to some of the information that is currently collected. This would

result in more accurate figures for N fixed and N balance, which are crucial for reliable

calculations of N losses such as nitrate leaching and emissions of the greenhouse gas

N2O. These are vital for refined predictions of the effects of strategic changes in the use of

legumes in farming systems. Ultimately this will lead to the development of better policies

to reduce the environmental impacts of European agriculture.




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REFERENCES

Bergersen, F.J., Turner, G.L., Gault, R.R., Peoples, M.B., Morthorpe, L.J. & Brockwell, J. 1992. Contributions of nitrogen in soybean crop residues to subsequent crops and to soils. Australian Journal of Agricultural Research 43: 155-169.

Britz, W. & Witzke, H.P. 2012. CAPRI Model Documentation 2012. www.capri-model.org/docs/capri_documentation.pdf (accessed Feb 2014).

Carlsson, G. & Huss-Danell, K. 2003. Nitrogen fixation in perennial forage legumes in the field. Plant and Soil 253: 353-372.

De Vries, W., Kros, J., Reinhardt, D.R., Wieggers, R., Velthof, G., Oudendag, D., Oenema, O., Nabuurs, G.J., Schelhaas, M.J., Perez Soba, M., Rienks, W., de Winter, W., van den Akker, J., Bakker, M., Verburg, P., Eickhout, B. & Bouman, L. 2011a. INTEGRATOR: A modelling tool for European-wide assessments of nitrogen and greenhouse gas fluxes in response to changes in land cover, land management and climate. Calculation procedures, application methodology and examples of scenario results. Alterra, Wageningen.

De Vries, W., Leip, A., Reinds, G.J., Kros, J., Lesschen, J.P. & Bouwman, A.F. 2011b. Comparison of land nitrogen budgets for European agriculture by various modeling approaches. Environmental Pollution 159: 3254-3268.

EEA 2008. Annual European Community Greenhouse Gas Inventory 1990-2006 and Inventory Report 2008. UNFCCC Secretariat, European Environment Agency.

Eurostat. 2014. Agriculture – agricultural production – crops products. <epp.eurostat.ec.europa.eu/portal/page/portal/agriculture/data/database>.

Evans, J., O'Connor, G.E., Turner, G.L., Coventry, D.R., Fettell, N., Mahoney, J., Armstrong, E.L. & Walsgott, D.N. 1989. N2 fixation and its value to soil N increase in lupin, field pea and other legumes in south-eastern Australia. Australian Journal of Agricultural Research 40: 791-805.

FAOstat. 2014. Crop production statistics. <faostat.fao.org>.

Fustec, J., Lesuffleur, F., Mahieu, S. & Cliquet, J.-B. 2010. Nitrogen rhizodeposition of legumes. A review. Agronomy for Sustainable Development 30: 57-66.

Golding, A.-L. & Dong, A. 2010. Hydrogen production by nitrogenase as a potential crop rotation benefit. Environmental Chemistry Letters 8: 101-121.

Green, C.J. & Blackmer, A.M. 1995. Residue decomposition effects on nitrogen availability to corn following corn or soybean. Soil Science Society of America Journal 59: 1065-1070.

Hardarson, G. & Atkins, C. 2003. Optimising biological N2 fixation by legumes in farming systems. Plant and Soil 252: 41-54.

Herridge, D.F., Marcellos, H., Felton, W.L., Turner, G.L. & Peoples, M.B. 1995. Chickpea increases soil-N fertility in cereal systems through nitrate sparing and N2 fixation. Soil Biology & Biochemistry 27: 545-551.

Herridge, D.F., Peoples, M.B. & Boddey, R.M. 2008. Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil 311: 1-18.




19

Hesterman, O.B., Russelle, M.P., Sheaffer, C.C. & Heichel, G.H. 1987. Nitrogen-utilization from fertilizer and legume residues in legume-corn rotations. Agronomy Journal 79: 726-731.

Jenkinson, D.S., Fox, R.H. & Rayner, J.H. 1985. Interactions between fertilizer nitrogen and soil-nitrogen - the so-called priming effect. Journal of Soil Science 36: 425-444.

Kurdali, F., Kalifa, K., AlShamma, M. 1997. Cultivar differences in nitrogen assimilation, partitioning and mobilization in rain-fed grown lentil. Field Crops Research 54: 235-243.

Kuzyakov, Y., Friedel, J.K., Stahr, K. 2000. Review of mechanisms and quantification of priming effects. Soil Biology & Biochemistry 32: 1485-1498.

Leip, A., Britz, W., Weiss, F. & De Vries, W. 2011. Farm, land, and soil nitrogen budgets for agriculture in Europe calculated with CAPRI. Environmental Pollution 159: 3243-3253

Liu, J., You, L., Amini, M., Obersteiner, M., Herrero, M., Zehnder, A.J. & Yang, H. 2010a. A high-resolution assessment on global nitrogen flows in cropland. Proceedings of the National Academy of Sciences of the United States of America 107: 8035-8040.

Liu, Y., Wu, L., Baddeley, J.A. & Watson, C.A. 2010b. Models of biological nitrogen fixation of legumes: A review. Agronomy for Sustainable Development 31: 155-172.

Mahieu, S., Fustec, J., Faure, M. L., Corre-Hellou, G., Crozat, Y. 2007. Comparison of two N-15 labelling methods for assessing nitrogen rhizodeposition of pea. Plant and Soil 295: 193-205.

Maimaiti, J., Zhang, Y., Yang, J., Cen, Y.-P., Layzell, D.B., Peoples, M. & Dong, Z. 2007. Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environmental Microbiology 9: 435-444.

Mariotti, F., Tome, D. & Mirand, P.P. 2008. Converting nitrogen into protein - beyond 6.25 and Jones' factors. Critical Reviews in Food Science and Nutrition 48: 177-184.

MNP. 2006. Integrated modelling of global environmental change. An overview of IMAGE 2.4. (Eds Bouwman, A.F., Kram, T. & Klein Goldewijk, K.) Netherlands Environmental Assessment Agency (MNP), Bilthoven, Netherlands.

Peoples, M.B., Brockwell, J., Herridge, D.F., Rochester, I.J., Alves, B.J.R., Urquiaga, S., Boddey, R.M., Dakora, F.D., Bhattarai, S., Maskey, S.L., Sampet, C., Rerkasem, B., Khan, D.F., Hauggaard-Nielsen, H. & Jensen, E.S. 2009. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48: 1-17.

Philippot, L. & Hallin, S. 2011. Towards food, feed and energy crops mitigating climate change. Trends in Plant Science 16: 476-480.

Pilbeam, C.J., Wood, M. & Jones, M.J. 1997. Proportion of total nitrogen and fixed nitrogen in shoots of lentil and chickpea grown in a Mediterranean-type environment. Experimental Agriculture 33: 139-148.

Schmidtke, K., Neumann, A., Hof, C., Rauber & R. 2004. Soil and atmospheric nitrogen uptake by lentil (Lens culinaris Medik.) and barley (Hordeum vulgare ssp. nudum L.) as monocrops and intercrops. Field Crops Research 87: 245-256.




20

Smil, V. 1999. Nitrogen in crop production: An account of global flows. Global Biogeochemical Cycles 13: 647-662.

Sosulski, F.W. & Holt, N.W. 1980. Amino-acid-composition and nitrogen-to-protein factors for grain legumes. Canadian Journal of Plant Science 60: 1327-1331.

Unkovich, M.J., Baldock, J. & Peoples, M.B. 2010. Prospects and problems of simple linear models for estimating symbiotic N2 fixation by crop and pasture legumes. Plant and Soil 329: 75-89.

Velthof, G. L., Oudendag, D., Witzke, H.R., Asman, W.A.H., Klimont, Z. & Oenema, O. 2009. Integrated assessment of nitrogen losses from agriculture in EU-27 using MITERRA-EUROPE. Journal of Environmental Quality 38: 402-417.

Vinther, F.P. & Dahlmann-Hansen, L. 2005. Effects of ridging on crop performance and symbiotic N2 fixation of fababean (Vicia faba L.). Soil Use and Management 21: 205-211.

Wichern, F., Eberhardt, E., Mayer, J., Joergensen, R.G. & Müller, T. 2008. Nitrogen rhizodeposition in agricultural crops: Methods, estimates and future prospects. Soil Biology and Biochemistry 40: 30-48.

Yang, J.Y., Drury, C.F., Yang, X.M., De Jong, R., Huffman, E.C., Campbell, C.A. & Kirkwood, V. 2010. Estimating biological N2 fixation in Canadian agricultural land using legume yields. Agriculture, Ecosystems and Environment 137: 192-201.




21

SUPPLEMENTARY TABLES

Supplementary Table 1. Areas (Eurostat, 2013), N retention, N fixation coefficients kfix and

N fixed by temporary and permanent grasslands in EU27 in 2009.

Country Area

(1000 ha)

N retention

(kg ha-1)

N fixation

coefficient

N fixed

(kg ha-1)

Total N fixed

(Gg)

Temp. Perm. Temp. Perm. kfix Temp. Perm. Temp. Perm. Total

Austria 156 1708 152 80 0.06 9.1 4.8 1.4 8.2 9.6

Belgium &

Luxembourg 103 580 257 198 0.06 15.4 11.9 1.6 6.9 8.5

Bulgaria 107 1906 30 42 0.08 2.4 3.3 0.3 6.3 6.6

Cyprus 28 14 39 30 0.05 2.0 1.5 0.05 0.02 0.08

Czech Republic 687 982 48 63 0.14 6.7 8.8 4.6 8.6 13.3

Denmark 475 216 149 157 0.14 20.9 21.9 9.9 4.7 14.6

Estonia 139 256 104 61 0.15 15.6 9.2 2.2 2.4 4.5

Finland 621 58 129 72 0.05 6.5 3.6 4.0 0.2 4.2

France 3433 9614 107 93 0.07 7.5 6.5 25.8 62.3 88.0

Germany 905 4784 159 159 0.08 12.8 12.7 11.5 60.7 72.2

Greece 281 1078 108 87 0.19 20.5 16.5 5.8 17.8 23.6

Hungary 174 1000 39 55 0.17 6.6 9.4 1.2 9.4 10.5

Ireland 586 3272 274 161 0.05 13.7 8.0 8.0 26.3 34.3

Italy 2333 3978 74 57 0.16 11.9 9.2 27.8 36.5 64.3

Lithuania 483 908 37 57 0.12 4.4 6.9 2.1 6.2 8.4

Latvia 402 714 54 62 0.07 3.8 4.3 1.5 3.1 4.6

Malta 4 0 45 43 0.05 2.3 2.2 0.009 0.000 0.009

Netherlands 196 848 364 225 0.05 18.2 11.2 3.6 9.5 13.1

Poland 1531 3420 90 64 0.07 6.3 4.5 9.7 15.4 25.1

Portugal 420 1264 92 54 0.05 4.6 2.7 1.9 3.4 5.4

Romania 801 4640 86 50 0.10 8.6 5.0 6.9 23.0 29.9

Slovak Republic 174 720 49 65 0.14 6.9 9.1 1.2 6.6 7.8

Slovenia 31 294 76 44 0.05 3.8 2.2 0.1 0.6 0.8

Spain 804 8464 84 58 0.07 5.9 4.0 4.8 34.1 38.9

Sweden 1096 452 169 84 0.11 18.6 9.3 20.4 4.2 24.6

UK 1159 9844 275 116 0.05 13.8 5.8 15.9 57.1 73.0




22

Supplementary Table 2. Constants (bold) and calculated values used to derive estimates

of fixed N and N balance for FAO classes of grain legumes. No constants were available

for the Pulses category, for which production-weighted means of the other categories were

used (82.15 for Total N, 53.85 for Fixed N and 7.71 for N balance). All calculated

quantities are relative to one tonne of grain production.

Commo

n bean

Faba

bean

Chick-

pea Lentil Lupins Pea

Soya

bean Vetches

Moisture content (g g-1) 0.140 0.140 0.140 0.140 0.140 0.140 0.140 0.140

Grain protein content (g g-1) 0.25 0.29 0.22 0.29 0.36 0.25 0.40 0.29

Protein to N 6.25 6.25 6.25 6.25 6.25 6.25 6.25 6.25

Grain N production (kg) 33.85 40.18 30.00 39.63 49.12 34.40 54.76 39.90

Harvest index 0.480 0.490 0.310 0.415 0.440 0.507 0.519 0.340

N harvest index 0.830 0.675 0.805 0.650 0.840 0.729 0.730 0.790

Above ground biomass (t) 1.792 1.755 2.774 2.072 1.955 1.696 1.657 2.529

Above-ground N production

(kg)

40.78 59.52 37.26 60.97 58.48 47.19 75.02 50.51

Root:shoot ratio 0.265 0.230 0.440 0.370 0.282 0.110 0.200 0.350

Root biomass production (t) 0.475 0.404 1.221 0.767 0.551 0.187 0.331 0.885

Root N content (g g-1) 0.022 0.022 0.014 0.014 0.012 0.022 0.017 0.029

Root N production (kg) 10.30 8.88 17.09 10.73 6.51 4.10 5.70 25.76

Proportional rhizodeposition 0.150 0.185 0.530 0.150 0.171 0.120 0.195 0.150

Rhizodeposition (kg) 7.66 12.66 28.81 10.76 11.11 6.16 15.74 11.44

Total N production (kg) 58.75 81.06 83.16 82.46 76.10 57.45 96.46 87.71

Proportion of N derived from

atmosphere, Ndfa 0.442 0.770 0.500 0.700 0.820 0.700 0.520 0.720

N fixed (kg) 26.0 62.4 41.6 57.7 62.4 40.2 50.2 63.2

N balance (kg) -7.9 22.2 11.6 18.1 13.3 5.8 -4.6 23.3




23

Supplementary Table 3. Calculated quantities of N fixed (t) by grain legume crops in EU27

in 2009.

Country Chickpea Common bean Faba bean Lentil Lupins Pea Soya bean Vetches

Austria 418 37 1395 3576 201

Belgium & Lux 19 169 253

Bulgaria 114 44 106 93 201 20 23

Cyprus 4 6 31 1 4 6

Czech Rep 162 137 2087 682 6

Denmark 901

Estonia 3 6 302

Finland 450

France 143 27295 775 512 21683 5508

Germany 2965 0 6671

Greece 112 570 156 162 44 109 613

Hungary 24 6 1 37 647 3591 2

Ireland 400

Italy 320 308 6104 84 893 23485 537

Latvia 62 105 6

Lithuania 93 318 661 917 95

Malta 10 46

Netherlands 114 393 101

Poland 740 967 3557 314 10 324

Portugal 27 52

Romania 3 580 1392 1206 4228

Slovakia 6 6 12 19 470 772 15

Slovenia 16 44 56 10

Spain 897 342 1741 687 281 5948 140 2588

Sweden 20 1629 1966

United Kingdom 42955 6080

Total 1484 3554 86872 1821 5267 52760 42024 4459




24

Supplementary Table 4. Crop production (FAO, 2013), and calculated quantities of total N

production, N fixed and the N balance for grain legume crops in the EU27 in 2009. All

figures in Gg.

Common

bean

Faba

bean

Chickpea Lentil Lupins Pea Soya

bean

Vetches Total

Crop

production 136 1392 35 32 84 1313 992 67 4051

N production 8.0 112.8 2.9 2.6 6.4 75.4 95.7 5.9 310

N fixed 3.5 86.9 1.5 1.8 5.3 52.8 49.8 4.2 206

N balance -1.1 31.0 0.4 0.6 1.1 7.6 -4.6 1.6 37

Supplementary Table 5. Sources of constants reported in Supplementary Table 2.

Common

bean

Faba

bean

Chickpea Lentil Lupins Pea Soya

bean

Vetches

Moisture correctiona default default default default default default default default

Grain protein content 1 1, 2 1 1 1, 2 1, 2 1, 3 4

Protein to N 5, 6 5, 6 5, 6 5, 6 5, 6 5, 6 5, 6 5, 6

Harvest index 7, 8, 9,

10, 11

12, 13,

14

15, 16 17 18, 19 20, 21, 22 23 4, 24

N harvest index 8 25, 26, 27 27, 28 28 29 30, 31 3 4, 32

Root:shoot ratio 33, 34 19, 35,

36, 37

38 39 19 31, 40,

41, 42

43, 44 32, 45

Root N content 33, 46 47,48 28 28 49 50, 51 23 32,52

Proportional

rhizodepositionb

default 54 27, 54 default 54 21, 31,

54

55 default

Ndfa 56, 57 58, 59 59, 60 59, 61,

62, 63,

64, 65

66 58, 59 3, 60, 23,

67

68, 69

a Default value for grains harvested dry was based on the typical industry reporting figure of 0.14. b Default value of 0.15 based on figures in 53 and 54.

1. U.S. Department of Agriculture, A. R. S. 2013. USDA National Nutrient Database for Standard Reference, Release 26. Nutrient Data Laboratory Home Page.

2. Annicchiarico, P. 2008. Adaptation of cool-season grain legume species across climatically-contrasting environments of southern Europe. Agronomy Journal 100, 1647-1654

3. Salvagiotti, F. et al. 2008. Nitrogen uptake, fixation and response to fertilizer N in soybeans: A review. Field Crops Research 108, 1-13

4. Larbi, A., Abd El-Moneim, A.M., Nakkoul, H., Jammal, B. & Hassan, S. 2011. Intra-species variations in yield and quality determinants in Vicia species: 3. Common vetch (Vicia sativa ssp. sativa L.). Animal Feed Science and Technology 164, 241-251

5. Mariotti, F., Tome, D. & Mirand, P.P. 2008. Converting nitrogen into protein - beyond 6.25 and Jones' factors. Critical Reviews in Food Science and Nutrition 48, 177-184




25

6. Sosulski, F.W. & Holt, N.W. 1980. Amino-acid-composition and nitrogen-to-protein factors for grain legumes. Canadian Journal of Plant Science 60, 1327-1331

7. Gebeyehu, S., Simane, B. & Kirkby, R. 2006. Genotype x cropping system interaction in climbing beans (Phaseolus vulgaris L.) grown as sole crop and in association with maize (Zea mays L.). European Journal of Agronomy 24, 396-403

8. Araujo, A.P. & Teixeira, M.G. 2012. Variability of nutrient harvest indices in common bean genotypes and their relationship with grain yield. Revista Brasileira de Ciencia do Solo 36, 137-146

9. Builes, V., Porch, T. & Harmsen, E. 2011. Genotypic differences in water use efficiency of common bean under drought stress. Agronomy Journal 103, 1206-1215

10. del Mar Alguacil, M., Roldan, A., Salinas-Garcia, J.R. & Ignacio Querejeta, J. 2011. No tillage affects the phosphorus status, isotopic composition and crop yield of Phaseolus vulgaris in a rain-fed farming system. Journal of the Science of Food and Agriculture 91, 268-272

11. Zafar, M. et al. 2011. Influence of integrated phosphorus supply and plant growth promoting rhizobacteria on growth, nodulation, yield and nutrient uptake in Phaseolus vulgaris. African Journal of Biotechnology 10, 16793-16807

12. Brereton, J.C., McGowan, M. & Dawkins, T.C.K. 1986. The relative sensitivity of spring barley, spring field beans and sugar beet crops to soil compaction. Field Crops Research 13, 223-237

13. Muñoz-Romero, V., López-Bellido, L. & López-Bellido, R.J. 2011. Faba bean root growth in a Vertisol: Tillage effects. Field Crops Research 120, 338-344

14. Confalone, A., Lizaso, J.I., Ruiz-Nogueira, B., Lopez-Cedron, F.X. & Sau, F. 2010. Growth, PAR use efficiency, and yield components of field-grown Vicia faba L. under different temperature and photoperiod regimes. Field Crops Research 115, 140-148

15. Siddique, K.H.M. & Sedgley, R.H. 1986. Chickpea (Cicer arietinum L), a potential grain legume for southwestern Australia - seasonal growth and yield. Australian Journal of Agricultural Research 37, 245-261

16. Malik, S.R., Bakhsh, A., Asif, M., Iqbal, U. & Iqbal, S. 2010. Assessment of genetic variability and interrelationship among some agronomic traits in chickpea. International Journal of Agriculture and Biology 12, 81-85

17. Zakeri, H. et al. 2012. Lentil performance in response to weather, no-till duration, and nitrogen in Saskatchewan. Agronomy Journal 104, 1501-1509

18. Sandaña, P. & Calderini, D.F. 2012. Comparative assessment of the critical period for grain yield determination of narrow-leafed lupin and pea. European Journal of Agronomy 40, 94-101

19. Gregory, P.J. 1998. Alternative crops for duplex soils: growth and water use of some cereal, legume, and oilseed crops, and pastures. Australian Journal of Agricultural Research 49, 21-32

20. Lecoeur, J. & Sinclair, T.R. 2001. Harvest index increase during seed growth of field pea. European Journal of Agronomy 14, 173-180

21. Arcand, M.M., Knight, J.D. & Farrell, R.E. 2013. Estimating belowground nitrogen inputs of pea and canola and their contribution to soil inorganic N pools using N-15 labeling. Plant and Soil 371, 67-80

22. Annicchiarico, P. 2007. Lucerne shoot and root traits associated with adaptation to favourable or drought-stress environments and to contrasting soil types. Field Crops Research 102, 51-59

23. Schweiger, P., Hofer, M., Hartl, W., Wanek, W. & Vollmann, J. 2012. N2 fixation by organically grown soybean in Central Europe: Method of quantification and agronomic effects. European Journal of Agronomy 41, 11-17

24. Firincioglu, H.K., Sabahaddin, Ü., Erbektas, E. & Dogruyol, L. 2010. Relationships between seed yield and yield components in common vetch (Vicia sativa ssp. sativa) populations sown in spring and autumn in central Turkey. Field Crops Research 116, 30-37

25. Brunner, H. & Zapata, F. 1984. Quantitative assessment of symbiotic nitrogen-fixation in diverse mutant lines of field bean (Vicia, faba, minor). Plant and Soil 82, 407-413

26. Li, C.J. et al. 2011. Crop nitrogen use and soil mineral nitrogen accumulation under different crop combinations and patterns of strip intercropping in northwest China. Plant and Soil 342, 221-231

27. Lopez-Bellido, L., itez-Vega, J., Garcia, P., Redondo, R. & Lopez-Bellido, R.J. 2011. Tillage system effect on nitrogen rhizodeposited by faba bean and chickpea. Field Crops Research 120, 189-195

28. Gan, Y. et al. 2010. Nitrogen accumulation in plant tissues and roots and N mineralization under oilseeds, pulses, and spring wheat. Plant and Soil 332, 451-461




26

29. Ayaz, S., McKenzie, B.A., Hill, G.D. & Mcneil, D.L. 2004. Nitrogen distribution in four grain legumes. Journal of Agricultural Science 142, 309-317

30. Lecoeur, J. & Sinclair, T.R. 2001. Nitrogen accumulation, partitioning, and nitrogen harvest index increase during seed fill of field pea. Field Crops Research 71, 87-99

31. Mahieu, S. et al. 2009. The influence of water stress on biomass and N accumulation, N partitioning between above and below ground parts and on N rhizodeposition during reproductive growth of pea (Pisum sativum L.). Soil Biology and Biochemistry 41, 380-387

32. Ozpinar, S. & Baytekin, H. 2006. Effects of tillage on biomass, roots, N-accumulation of vetch (Vicia sativa L.) on a clay loam soil in semi-arid conditions. Field Crops Research 96, 235-242

33. Fernández-Luqueño, V. et al. 2010. Effect of different nitrogen sources on plant characteristics and yield of common bean (Phaseolus vulgaris L.). Bioresource Technology 101, 396-403

34. Andrews, M., Sprent, J.I., Raven, J.A. & Eady, P.E. 1999. Relationships between shoot to root ratio, growth and leaf soluble protein concentration of Pisum sativum, Phaseolus vulgaris and Triticum aestivum under different nutrient deficiencies. Plant, Cell & Environment 22, 949-958

35. Vinther, F.P. & Dahlmann-Hansen, L. 2005. Effects of ridging on crop performance and symbiotic N2 fixation of fababean (Vicia faba L.). Soil Use and Management 21, 205-211

36. Rengasamy, J.I. & Reid, J.B. 1993. Root system modification of faba beans (Vicia faba L.), and its effects on crop performance. 1. Responses of root and shoot growth to subsoiling, irrigation and sowing date. Field Crops Research 33, 175-196

37. Crawford, M.C., Grace, P.R., Bellotti, W.B.D. & Oades, J.M. 1997. Root production of a barrel medic (Medicago truncatula) pasture, a barley grass (Hordeum leporinum) pasture, and a faba bean (Vicia faba) crop in southern Australia. Australian Journal of Agricultural Research 48, 1139-1150

38. Gan, Y. & Liang, B. 2010. Ratios of carbon mass in nodules to other plant tissues in chickpea. Plant and Soil 332, 257-266

39. Hobson, K., Armstrong, R., Nicolas, M., Connor, D. & Materne, M. 2006. Response of lentil (Lens culinaris) germplasm to high concentrations of soil boron. Euphytica 151, 371-382

40. McPhee, K. 2005. Variation for seedling root architecture in the core collection of pea germplasm. Crop Science 45, 1758-1763

41. Baddeley, J.A. & Henderson, T.J. 2011. Characterisation of key above- and below-ground parameters of different pea cultivars. Aspects of Applied Biology 109, 161-164

42. Gan, Y., Liang, B., Liu, L., Wang, X. & McDonald, C. 2011. C:N ratios and carbon distribution profile across rooting zones in oilseed and pulse crops. Crop & Pasture Science 62, 496-503

43. Yang, J.Y. et al. 2010. Estimating biological N2 fixation in Canadian agricultural land using legume yields. Agriculture Ecosystems & Environment 137, 192-201

44. Gerardo, R., Gutierrez Boem, F.H. & Fernandez, M.C. 2013. Severe phosphorus stress affects sunflower and maize but not soybean root to shoot allometry. Agronomy Journal 105, 1283-1288

45. Mariotti, M., Masoni, A., Ercoli, L. & Arduini, I. 2009. Above- and below-ground competition between barley, wheat, lupin and vetch in a cereal and legume intercropping system. Grass and Forage Science 64, 401-412

46. Mortimer, P., Perez-Fernandez, M. & Valentine, A. 2009. Arbuscular mycorrhizae affect the N and C economy of nodulated Phaseolus vulgaris (L.) during NH4

+ nutrition. Soil Biology & Biochemistry 41, 2115-2121

47. Lopez-Bellido, F.J., Lopez-Bellido, R.J., Redondo, R. & Lopez-Bellido, L. 2010. B value and isotopic fractionation in N2 fixation by chickpea (Cicer arietinum L.) and faba bean (Vicia faba L.). Plant and Soil 337, 425-434

48. Mauromicale, G. et al. 2005. Root nodulation and nitrogen accumulation and partitioning in legume crops as affected by soil solarization. Plant and Soil 271, 275-284

49. McNeill, A.M. & Fillery, I.R.P. 2008. Field measurement of lupin belowground nitrogen accumulation and recovery in the subsequent cereal-soil system in a semi-arid Mediterranean-type climate. Plant and Soil 302, 297-316

50. Ludidi, N.N. et al. 2007. Genetic variation in pea (Pisum sativum L.) demonstrates the importance of root but not shoot C/N ratios in the control of plant morphology and reveals a unique relationship between shoot length and nodulation intensity. Plant Cell and Environment 30, 1256-1268

51. Voisin, A.S., Salon, C., Munier-Jolain, N.G. & Ney, B. 2002. Effect of mineral nitrogen on nitrogen nutrition and biomass partitioning between the shoot and roots of pea (Pisum sativum L.). Plant and Soil 242, 251-262




27

52. Pederson, G.A., Brink, G.E. & Fairbrother, T.E. 2002. Nutrient uptake in plant parts of sixteen forages fertilized with poultry litter: Nitrogen, phosphorus, potassium, copper, and zinc. Agronomy Journal 94, 895-904

53. Mahieu, S., Fustec, J., Faure, M.L., Corre-Hellou, G. & Crozat, Y. 2007. Comparison of two N-15 labelling methods for assessing nitrogen rhizodeposition of pea. Plant and Soil 295, 193-205

54. Wichern, F., Eberhardt, E., Mayer, J., Joergensen, R.G. & Müller, T. 2008. Nitrogen rhizodeposition in agricultural crops: Methods, estimates and future prospects. Soil Biology & Biochemistry 40, 30-48

55. Laberge, G., Franke, A., Ambus, P. & Hogh-Jensen, H. 2009. Nitrogen rhizodeposition from soybean (Glycine max) and its impact on nutrient budgets in two contrasting environments of the Guinean savannah zone of Nigeria. Nutrient Cycling in Agroecosystems 84, 49-58

56. Chagas, E., Araujo, A.P., Alves, B.J.R. & Teixeira, M. G. 2010. Seeds enriched with phosphorus and molybdenum improve the contribution of biological nitrogen fixation to common bean as estimated by N-15 isotope dilution. Revista Brasileira de Ciencia do Solo 34, 1093-1101

57. Hardarson, G. et al. 1993. Genotypic variation in biological nitrogen-fixation by common bean. Plant and Soil 152, 59-70

58. Peoples, M.B. et al. 2009. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48, 1-17

59. Rennie, R.J. & Dubetz, S. 1986. N-15 - determined nitrogen-fixation in field-grown chickpea, lentil, fababean, and field pea. Agronomy Journal 78, 654-660

60. Hardarson, G. & Atkins, C. 2003. Optimising biological N2 fixation by legumes in farming systems. Plant and Soil 252, 41-54

61. Schmidtke, K., Neumann, A., Hof, C. & Rauber, R. 2004. Soil and atmospheric nitrogen uptake by lentil (Lens culinaris Medik.) and barley (Hordeum vulgare ssp. nudum L.) as monocrops and intercrops. Field Crops Research 87, 245-256

62. Hafeez, F.Y., Shah, N.H. & Malik, K.A. 2000. Field evaluation of lentil cultivars inoculated with Rhizobium leguminosarum bv. viciae strains for nitrogen fixation using nitrogen-15 isotope dilution. Biology and Fertility of Soils 31, 65-69

63. Haynes, R.J., Martin, R.J. & Goh, K.M. 1993. Nitrogen-fixation, accumulation of soil-nitrogen and nitrogen-balance for some field-grown legume crops. Field Crops Research 35, 85-92

64. Kurdali, F., Kalifa, K. & AlShamma, M. 1997. Cultivar differences in nitrogen assimilation, partitioning and mobilization in rain-fed grown lentil. Field Crops Research 54, 235-243

65. Shah, Z., Shah, S.H., Peoples, M.B., Schwenke, G.D. & Herridge, D.F. 2003. Crop residue and fertiliser N effects on nitrogen fixation and yields of legume-cereal rotations and soil organic fertility. Field Crops Research 83, 1-11

66. Unkovich, M.J., Pate, J.S., Armstrong, E.L. & Sanford, P. 1995. Nitrogen economy of annual crop and pasture legumes in southwest Australia. Soil Biology & Biochemistry 27, 585-588

67. Bohm, G.M.B. et al. 2009. Glyphosate- and imazethapyr-induced effects on yield, nodule mass and biological nitrogen fixation in field-grown glyphosate-resistant soybean. Soil Biology & Biochemistry 41, 420-422

68. Mueller, T. & Thorup-Kristensen, K. 2001. N-fixation of selected green manure plants in an organic crop rotation. Biological Agriculture and Horticulture 18, 345-363

69. Papastylianou, I. & Danso, S.K.A. 1991. Nitrogen-fixation and transfer in vetch and vetch-oats mixtures. Soil Biology & Biochemistry 23, 447-452

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